Impaired neutrophil extracellular trap formation: a novel defect in the innate immune system of aged individuals

Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in hu...

Full description

Saved in:
Bibliographic Details
Published inAging cell Vol. 13; no. 4; pp. 690 - 698
Main Authors Hazeldine, Jon, Harris, Phillipa, Chapple, Iain L., Grant, Melissa, Greenwood, Hannah, Livesey, Amy, Sapey, Elizabeth, Lord, Janet M.
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.08.2014
BlackWell Publishing Ltd
Subjects
Acetic acid
Adult
Age
Aged
Aging
Aging - immunology
Aging - pathology
Analysis
Bacteria
Case-Control Studies
Chronic Disease
CXCR2 protein
Defects
Disease susceptibility
Enzyme Activation - drug effects
Enzymes
Extracellular Traps - drug effects
Extracellular Traps - immunology
Female
Gum disease
Health aspects
Humans
Hypochlorous acid
Immune response
Immune system
Immunity, Innate - drug effects
Immunity, Innate - immunology
Infection
Infections
Innate immunity
Interleukin-8 - metabolism
Kinases
Leukocytes (neutrophilic)
Lipopolysaccharides
Lipopolysaccharides - pharmacology
Male
MAP kinase
Medical research
Medicine, Experimental
Microscopy
Middle Aged
neutrophil
neutrophil extracellular traps
Neutrophils
Neutrophils - drug effects
Neutrophils - immunology
Older people
Original
p38 Mitogen-Activated Protein Kinases - metabolism
Pathogens
Periodontitis
Periodontitis - immunology
Periodontitis - pathology
Proteins
Reactive oxygen species
Reactive Oxygen Species - metabolism
Receptors, Cell Surface - metabolism
Risk factors
TLR4 protein
Toll-like receptors
Tumor necrosis factor
Tumor Necrosis Factor-alpha - pharmacology
Tumor necrosis factor-TNF
neutrophil extracellular traps
aging
neutrophil
periodontitis
Online AccessGet full text
ISSN1474-9718
1474-9726
1474-9726
DOI10.1111/acel.12222

Cover

Abstract Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF‐α‐primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)‐ and interleukin‐8 (IL‐8)‐induced NET formation exhibits a significant age‐related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL‐8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol‐12‐myristate‐13‐acetate (PMA) showed no age‐associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age‐related decline in NET and ROS generation. TNF‐α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age‐matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
AbstractList Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF‐α‐primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)‐ and interleukin‐8 (IL‐8)‐induced NET formation exhibits a significant age‐related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL‐8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol‐12‐myristate‐13‐acetate (PMA) showed no age‐associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age‐related decline in NET and ROS generation. TNF‐α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age‐matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF‐α‐primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)‐ and interleukin‐8 (IL‐8)‐induced NET formation exhibits a significant age‐related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL‐8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol‐12‐myristate‐13‐acetate (PMA) showed no age‐associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age‐related decline in NET and ROS generation. TNF‐α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age‐matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF-α-primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)- and interleukin-8 (IL-8)-induced NET formation exhibits a significant age-related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL-8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol-12-myristate-13-acetate (PMA) showed no age-associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age-related decline in NET and ROS generation. TNF-α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age-matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF-α-primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)- and interleukin-8 (IL-8)-induced NET formation exhibits a significant age-related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL-8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol-12-myristate-13-acetate (PMA) showed no age-associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age-related decline in NET and ROS generation. TNF-α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age-matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF-[alpha]-primed neutrophils generate significantly more NETs than unprimed neutrophils and that lipopolysaccharide (LPS)- and interleukin-8 (IL-8)-induced NET formation exhibits a significant age-related decline. NET formation requires generation of reactive oxygen species (ROS), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL-8 receptors (CXCR1 and CXCR2) and the LPS receptor TLR4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol-12-myristate-13-acetate (PMA) showed no age-associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age-related decline in NET and ROS generation. TNF-[alpha] priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NETs in response to PMA and hypochlorous acid (HOCL). Neutrophil extracellular trap generation to HOCL, but not PMA, was lower in older periodontitis patients but not in comparison with age-matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
Neutrophil extracellular traps ( NET s) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response against rapidly dividing bacteria. Although older adults are more susceptible to such infections, no study has examined whether aging in humans influences NET formation. We report that TNF ‐α‐primed neutrophils generate significantly more NET s than unprimed neutrophils and that lipopolysaccharide ( LPS )‐ and interleukin‐8 ( IL ‐8)‐induced NET formation exhibits a significant age‐related decline. NET formation requires generation of reactive oxygen species ( ROS ), and this was also reduced in neutrophils from older donors identifying a mechanism for reduced NET formation. Expression of IL ‐8 receptors ( CXCR 1 and CXCR 2) and the LPS receptor TLR 4 was similar on neutrophils from young and old subjects, and neutrophils challenged with phorbol‐12‐myristate‐13‐acetate ( PMA ) showed no age‐associated differences in ROS or NET production. Taken together, these data suggest a defect in proximal signalling underlies the age‐related decline in NET and ROS generation. TNF ‐α priming involves signalling through p38 MAP kinase, but activation kinetics were comparable in neutrophils from young and old donors. In a clinical setting, we assessed the capacity of neutrophils from young and older patients with chronic periodontitis to generate NET s in response to PMA and hypochlorous acid ( HOCL ). Neutrophil extracellular trap generation to HOCL , but not PMA , was lower in older periodontitis patients but not in comparison with age‐matched controls. Impaired NET formation is thus a novel defect of innate immunity in older adults but does not appear to contribute to the increased incidence of periodontitis in older adults.
Audience Academic
Author Grant, Melissa
Harris, Phillipa
Chapple, Iain L.
Greenwood, Hannah
Lord, Janet M.
Livesey, Amy
Sapey, Elizabeth
Hazeldine, Jon
Author_xml – sequence: 1
  givenname: Jon
  surname: Hazeldine
  fullname: Hazeldine, Jon
  organization: Birmingham University Medical School
– sequence: 2
  givenname: Phillipa
  surname: Harris
  fullname: Harris, Phillipa
  organization: University of Birmingham
– sequence: 3
  givenname: Iain L.
  surname: Chapple
  fullname: Chapple, Iain L.
  organization: University of Birmingham
– sequence: 4
  givenname: Melissa
  surname: Grant
  fullname: Grant, Melissa
  organization: University of Birmingham
– sequence: 5
  givenname: Hannah
  surname: Greenwood
  fullname: Greenwood, Hannah
  organization: University of Birmingham
– sequence: 6
  givenname: Amy
  surname: Livesey
  fullname: Livesey, Amy
  organization: Birmingham University Medical School
– sequence: 7
  givenname: Elizabeth
  surname: Sapey
  fullname: Sapey, Elizabeth
  organization: University of Birmingham
– sequence: 8
  givenname: Janet M.
  surname: Lord
  fullname: Lord, Janet M.
  organization: Birmingham University Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24779584$$D View this record in MEDLINE/PubMed
BookMark eNqNkl1rFDEUhgep2A-98QdIwBsRdk0ymXx4ISxL1cKCN3od0snJbspMMmZmVvffm-m2ZVvKYnJxDslz3iQn73lxEmKAonhL8Jzk8cnU0MwJzeNFcUaYYDMlKD95yIk8Lc77_gZjIhQuXxWnlAmhKsnOiu6q7YxPYFGAcUix2_gGwd8hTaLN2JiEct4hF1NrBh_DZ2RQiFtokAUH9YB8QMMGcghmyKFtxwCo3_UDtCg6ZNZZ2wfrt96OpulfFy9dDvDmLl4Uv75e_lx-n61-fLtaLlazmgtOZ0SCJIIIzqwlpeEUKuKYNBURjpRCiWtCDbYgHVhRVoZIbkxlFXYVgRJUeVF82et243ULtoaQ39HoLvnWpJ2OxuvHO8Fv9DpuNSspV4xmgQ93Ain-HqEfdOv7qSkmQBx7TSqmeMmk4Bl9_wS9iWMK-Xm6pFRIwjg-SmUtKQRh5QG1Ng1oH1yc_mI6Wi8k40oRTNVRSuBKyArTKlPzZ6g8LbS-ziZyPq8_kv2vgsMT3h12-aG99wbLAN4DdYp9n8Dp2g-3RsrKvtEE68nDerKbvvVwLvn4pORe9VmY7OE_-Wa7I6ReLC9X-5p_lK7-pw
CitedBy_id crossref_primary_10_1093_ageing_afab026
crossref_primary_10_1128_IAI_00653_20
crossref_primary_10_1177_0022034515609097
crossref_primary_10_3310_eme07100
crossref_primary_10_1111_bph_15671
crossref_primary_10_1021_acs_molpharmaceut_8b01342
crossref_primary_10_1038_s41418_018_0261_x
crossref_primary_10_3389_fimmu_2019_00635
crossref_primary_10_3389_fimmu_2023_1167404
crossref_primary_10_3389_fimmu_2020_579220
crossref_primary_10_1111_imr_13153
crossref_primary_10_1093_jleuko_qiad101
crossref_primary_10_1016_j_biomaterials_2021_120827
crossref_primary_10_4049_jimmunol_1600766
crossref_primary_10_1016_j_celrep_2017_02_004
crossref_primary_10_1016_j_it_2017_08_004
crossref_primary_10_1371_journal_ppat_1008497
crossref_primary_10_1007_s11357_023_00835_0
crossref_primary_10_3389_fimmu_2021_681449
crossref_primary_10_4049_immunohorizons_1900026
crossref_primary_10_1097_MD_0000000000039342
crossref_primary_10_3389_fimmu_2022_1051140
crossref_primary_10_31487_j_ORD_2019_01_02
crossref_primary_10_1111_prd_12454
crossref_primary_10_18632_oncotarget_2856
crossref_primary_10_3389_fphar_2024_1421598
crossref_primary_10_3389_fmars_2021_690879
crossref_primary_10_1007_s10522_015_9614_8
crossref_primary_10_1128_IAI_00327_18
crossref_primary_10_1371_journal_pone_0253698
crossref_primary_10_1007_s00262_016_1921_7
crossref_primary_10_1016_j_jaut_2024_103169
crossref_primary_10_3389_fimmu_2020_571085
crossref_primary_10_3389_fragi_2021_748591
crossref_primary_10_1089_ars_2023_0365
crossref_primary_10_3390_ijms231911845
crossref_primary_10_1016_j_autrev_2021_102893
crossref_primary_10_1016_j_cell_2021_03_005
crossref_primary_10_1101_cshperspect_a041197
crossref_primary_10_3390_ijms22020821
crossref_primary_10_1016_j_exger_2017_12_020
crossref_primary_10_1684_ecn_2020_0441
crossref_primary_10_1002_JLB_1HI1120_779R
crossref_primary_10_2147_IJN_S244849
crossref_primary_10_3389_fmed_2020_589553
crossref_primary_10_1016_j_bbi_2016_02_024
crossref_primary_10_1007_s11904_021_00547_0
crossref_primary_10_1111_omi_12099
crossref_primary_10_1021_acs_analchem_5b03827
crossref_primary_10_1371_journal_pone_0298425
crossref_primary_10_1073_pnas_1719978115
crossref_primary_10_1016_j_arr_2022_101768
crossref_primary_10_18632_aging_101303
crossref_primary_10_1371_journal_pone_0176472
crossref_primary_10_1002_cre2_803
crossref_primary_10_3389_fneur_2021_811518
crossref_primary_10_3389_fimmu_2018_01269
crossref_primary_10_1111_prd_12126
crossref_primary_10_3389_fnagi_2022_1041333
crossref_primary_10_1007_s40266_024_01100_5
crossref_primary_10_3389_fragi_2022_818700
crossref_primary_10_1016_j_arr_2015_02_005
crossref_primary_10_1016_j_cger_2017_06_002
crossref_primary_10_1016_j_vetimm_2015_10_014
crossref_primary_10_1186_s40035_023_00369_7
crossref_primary_10_3390_cells11182901
crossref_primary_10_1371_journal_pone_0191231
crossref_primary_10_1007_s40520_022_02201_0
crossref_primary_10_17159_sajs_2016_20150072
crossref_primary_10_1164_rccm_201812_2328OC
crossref_primary_10_1097_CM9_0000000000003410
crossref_primary_10_1016_j_intimp_2021_108516
crossref_primary_10_1007_s00441_017_2751_4
crossref_primary_10_1186_s12916_022_02564_1
crossref_primary_10_1002_art_40314
crossref_primary_10_1161_CIRCRESAHA_118_310966
crossref_primary_10_1177_1756284820974913
crossref_primary_10_1101_cshperspect_a041324
crossref_primary_10_1002_JLB_3A1017_398RR
crossref_primary_10_1016_j_arr_2021_101541
crossref_primary_10_1002_JLB_3MR0822_645RR
crossref_primary_10_1093_gerona_glaa291
crossref_primary_10_1055_a_2444_3422
crossref_primary_10_1016_j_molimm_2015_01_015
crossref_primary_10_1111_prd_12380
crossref_primary_10_1038_s41598_019_42762_1
crossref_primary_10_1002_iid3_1209
crossref_primary_10_1186_s12871_019_0911_7
crossref_primary_10_3389_fimmu_2020_01748
crossref_primary_10_1007_s10522_018_9771_7
crossref_primary_10_1093_cvr_cvz084
crossref_primary_10_3390_biomedicines12081890
crossref_primary_10_3389_fcimb_2017_00217
crossref_primary_10_1016_j_exger_2024_112365
crossref_primary_10_3390_nu13010051
crossref_primary_10_1161_ATVBAHA_117_309580
crossref_primary_10_3389_fimmu_2024_1353106
crossref_primary_10_1016_j_arr_2021_101553
crossref_primary_10_1038_s41368_024_00332_w
crossref_primary_10_1164_rccm_201603_0596OC
crossref_primary_10_1158_0008_5472_CAN_20_4125
crossref_primary_10_1080_08923973_2022_2088386
crossref_primary_10_1186_1745_6215_15_332
crossref_primary_10_3390_ijerph17103567
crossref_primary_10_36150_2499_6564_N580
crossref_primary_10_1155_2018_4065362
crossref_primary_10_1016_j_biomaterials_2020_120389
crossref_primary_10_1016_j_pharmthera_2020_107529
crossref_primary_10_3390_ijms242316904
crossref_primary_10_3389_fcell_2018_00109
crossref_primary_10_3390_ijms221810106
crossref_primary_10_1016_j_cger_2016_02_007
crossref_primary_10_3233_HAB_160293
crossref_primary_10_3390_jcm12030976
crossref_primary_10_1182_blood_2015_01_624023
crossref_primary_10_1164_rccm_201704_0814OC
crossref_primary_10_1093_ofid_ofad384
crossref_primary_10_3389_fneur_2022_854390
crossref_primary_10_1016_j_bioorg_2023_107051
crossref_primary_10_1093_ecco_jcc_jjad025
crossref_primary_10_1016_j_mib_2015_11_003
crossref_primary_10_1016_j_arr_2017_01_006
crossref_primary_10_3390_cells11213521
crossref_primary_10_1016_j_intimp_2022_109625
crossref_primary_10_1016_j_jaci_2022_12_004
crossref_primary_10_3389_fragi_2023_1234572
crossref_primary_10_1017_erm_2022_12
crossref_primary_10_1189_jlb_5MR0315_104R
crossref_primary_10_1080_21505594_2021_1939608
crossref_primary_10_1136_thoraxjnl_2020_215986
crossref_primary_10_1590_0001_3765201720160487
crossref_primary_10_3389_fimmu_2020_573662
crossref_primary_10_1016_j_smim_2021_101506
crossref_primary_10_1088_1742_6596_1664_1_012124
crossref_primary_10_3389_fimmu_2019_00012
crossref_primary_10_3389_fragi_2021_708788
crossref_primary_10_36740_WLek202209103
crossref_primary_10_1016_j_clim_2018_04_002
crossref_primary_10_1007_s11357_025_01517_9
crossref_primary_10_1186_s13075_018_1624_x
crossref_primary_10_1136_thorax_2024_222215
crossref_primary_10_3389_fimmu_2022_888415
crossref_primary_10_1016_j_exger_2022_111955
crossref_primary_10_1074_jbc_RA118_005280
crossref_primary_10_1136_thoraxjnl_2018_212826
crossref_primary_10_1007_s12035_024_04464_2
crossref_primary_10_1016_j_arr_2015_10_003
crossref_primary_10_1093_braincomms_fcae452
crossref_primary_10_1016_j_intimp_2022_109397
crossref_primary_10_1093_gerona_glw062
crossref_primary_10_1002_iub_2379
crossref_primary_10_1160_TH16_09_0704
crossref_primary_10_3390_cells10030494
crossref_primary_10_1111_cei_12863
crossref_primary_10_1016_j_prp_2022_153896
crossref_primary_10_1111_jcpe_12675
crossref_primary_10_3389_fimmu_2020_00729
crossref_primary_10_3389_fimmu_2022_949928
crossref_primary_10_1002_advs_202001940
crossref_primary_10_1038_s43587_021_00086_8
crossref_primary_10_1038_s41385_018_0115_3
crossref_primary_10_1093_cvr_cvab329
crossref_primary_10_1016_j_cbi_2015_04_011
crossref_primary_10_1182_bloodadvances_2018030585
crossref_primary_10_3390_cells8090946
crossref_primary_10_1016_j_tranon_2024_102072
crossref_primary_10_1038_s41392_023_01502_8
crossref_primary_10_3389_fragi_2024_1426436
crossref_primary_10_1177_1753425916631404
crossref_primary_10_3389_fimmu_2023_1253964
crossref_primary_10_3389_fimmu_2019_00423
crossref_primary_10_1016_j_arr_2020_101071
crossref_primary_10_1007_s40266_019_00684_7
crossref_primary_10_1111_cei_12881
crossref_primary_10_3390_ijms18122612
crossref_primary_10_1093_bfgp_elab009
crossref_primary_10_1084_jem_20220011
crossref_primary_10_1016_j_archoralbio_2019_03_029
crossref_primary_10_3389_fimmu_2016_00250
crossref_primary_10_3389_fimmu_2018_00359
crossref_primary_10_1089_ars_2020_8021
crossref_primary_10_1016_j_smim_2022_101631
crossref_primary_10_3389_fimmu_2024_1330536
crossref_primary_10_1016_j_fsi_2021_08_023
crossref_primary_10_1111_imm_12740
crossref_primary_10_3390_biomedicines11082252
crossref_primary_10_3389_fcimb_2021_651474
crossref_primary_10_3389_fonc_2022_992056
crossref_primary_10_3390_cells11030359
crossref_primary_10_1186_s12979_017_0104_5
crossref_primary_10_1159_000452615
crossref_primary_10_1002_mco2_70048
crossref_primary_10_4110_in_2019_19_e37
crossref_primary_10_1080_10717544_2021_2018523
crossref_primary_10_15252_embr_201948777
crossref_primary_10_1016_j_pharmthera_2020_107799
crossref_primary_10_1089_vim_2023_0045
crossref_primary_10_1155_2017_8148742
crossref_primary_10_3390_biomedicines10040773
crossref_primary_10_1152_physrev_00062_2021
crossref_primary_10_1111_bph_15759
crossref_primary_10_3389_fdmed_2022_844865
Cites_doi 10.1016/j.vaccine.2010.12.121
10.1038/nm.1959
10.1042/cs0700059
10.1083/jcb.200606027
10.1111/j.1462-5822.2005.00659.x
10.1073/pnas.1200419109
10.1159/000203700
10.1371/journal.pone.0041454
10.1002/jlb.67.1.40
10.1038/nm.2847
10.1902/jop.1994.65.3.260
10.1182/blood-2008-07-171629
10.4049/jimmunol.181.8.5775
10.1016/j.bbrc.2011.08.052
10.1189/jlb.0711387
10.1902/jop.2008.080173
10.1038/sj.bdj.2012.1088
10.1182/blood-2009-05-221606
10.1083/jcb.200806072
10.1073/pnas.0900226106
10.1086/322685
10.1111/prd.12025
10.1016/j.mad.2004.06.001
10.1016/S0022-1759(99)00146-5
10.1038/cdd.2011.1
10.1016/S0021-9258(19)36655-4
10.1126/science.1092385
10.1074/jbc.M405883200
10.1111/j.1474-9728.2004.00110.x
10.1111/j.1365-2249.2011.04518.x
10.1189/jlb.70.6.881
10.1186/cc11442
10.1371/journal.pone.0066407
10.1136/annrheumdis-2012-202701
10.1182/blood-2011-07-364604
10.1172/JCI27544
10.1111/j.1365-2141.2007.06880.x
10.1002/jlb.64.4.537
10.4049/jimmunol.1103414
10.1590/S1678-77572012000500002
10.1086/374621
ContentType Journal Article
Copyright 2014 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd.
2014 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.
COPYRIGHT 2014 John Wiley & Sons, Inc.
Copyright © 2014 The Anatomical Society and John Wiley & Sons Ltd
2014. This work is published under https://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2014 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd. 2014
Copyright_xml – notice: 2014 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd.
– notice: 2014 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.
– notice: COPYRIGHT 2014 John Wiley & Sons, Inc.
– notice: Copyright © 2014 The Anatomical Society and John Wiley & Sons Ltd
– notice: 2014. This work is published under https://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2014 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd. 2014
DBID 24P
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7QP
7TK
8FE
8FH
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
GNUQQ
HCIFZ
LK8
M7P
PHGZM
PHGZT
PIMPY
PKEHL
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
5PM
DOI 10.1111/acel.12222
DatabaseName Wiley Online Library Open Access
CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Calcium & Calcified Tissue Abstracts
Neurosciences Abstracts
ProQuest SciTech Collection
ProQuest Natural Science Collection
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Database
ProQuest Central
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
ProQuest Central Student
SciTech Premium Collection
Biological Sciences
Biological Science Database
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database
ProQuest One Academic Middle East (New)
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Biological Science Collection
ProQuest Central Essentials
ProQuest One Academic Eastern Edition
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
Biological Science Database
ProQuest SciTech Collection
Neurosciences Abstracts
ProQuest Central China
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Academic UKI Edition
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest Central (New)
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
ProQuest One Academic (New)
MEDLINE - Academic
DatabaseTitleList

MEDLINE

MEDLINE - Academic
Publicly Available Content Database
Publicly Available Content Database



CrossRef
Database_xml – sequence: 1
  dbid: 24P
  name: Wiley Open Access
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 1474-9726
EndPage 698
ExternalDocumentID PMC4326942
3386178091
A846991029
A705785025
24779584
10_1111_acel_12222
ACEL12222
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: Biotechnology and Biological sciences Research Council
– fundername: Medical Research Council
  grantid: 1090321
– fundername: Biotechnology and Biological Sciences Research Council
– fundername: Medical Research Council
  grantid: MR/L008335/1
GroupedDBID ---
.3N
.GA
.Y3
05W
0R~
10A
1OC
23M
24P
2WC
31~
36B
4.4
50Y
50Z
51W
51X
52M
52N
52O
52P
52R
52S
52T
52W
52X
53G
5GY
5HH
5LA
5VS
66C
6J9
702
7PT
8-0
8-1
8-3
8-4
8-5
8FE
8FH
8UM
930
A01
A03
AAMMB
AAZKR
ABCQN
ABDBF
ABEML
ABJNI
ACCMX
ACGFO
ACGFS
ACPRK
ACSCC
ACUHS
ACXQS
ADBBV
ADKYN
ADRAZ
ADZMN
AEFGJ
AEGXH
AENEX
AFBPY
AFEBI
AFKRA
AFZJQ
AGXDD
AIAGR
AIDQK
AIDYY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AOIJS
AVUZU
BAWUL
BBNVY
BCNDV
BENPR
BFHJK
BHPHI
BY8
CAG
CCPQU
COF
CS3
D-6
D-7
D-E
D-F
DIK
DR2
E3Z
EAD
EAP
EBD
EBS
EJD
EMB
EMK
EMOBN
EST
ESX
F00
F01
F04
F5P
FIJ
GODZA
GROUPED_DOAJ
GX1
HCIFZ
HF~
HOLLA
HZ~
IAO
IHE
IHR
ITC
IX1
J0M
K.9
KQ8
LC2
LC3
LH4
LK8
LP6
LP7
LW6
M48
M7P
MK4
N04
N05
N9A
O9-
OBS
OIG
OK1
OVD
P2P
P2X
P2Z
P4B
P4D
PHGZM
PHGZT
PIMPY
PQGLB
Q11
ROL
RPM
RX1
SUPJJ
SV3
TEORI
TR2
TUS
UB1
V8K
W8V
WIN
WQJ
WXI
XG1
YFH
YUY
~IA
~WT
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
AAHHS
ACCFJ
ADZOD
AEEZP
AEQDE
AIWBW
AJBDE
PMFND
7QP
7TK
ABUWG
AZQEC
DWQXO
GNUQQ
PKEHL
PQEST
PQQKQ
PQUKI
PRINS
7X8
5PM
ID FETCH-LOGICAL-c6762-18e8171764dd13a62e51f48a517f13797b12a0de8fed735a186aa5d90f51e3e93
IEDL.DBID M48
ISSN 1474-9718
1474-9726
IngestDate Thu Aug 21 18:31:48 EDT 2025
Tue Aug 05 09:52:37 EDT 2025
Sun Jul 27 14:16:50 EDT 2025
Wed Aug 13 03:06:30 EDT 2025
Wed Jul 16 16:53:06 EDT 2025
Tue Jun 17 21:24:52 EDT 2025
Tue Jul 15 03:51:22 EDT 2025
Tue Jun 10 20:31:53 EDT 2025
Mon Jul 21 06:05:48 EDT 2025
Thu Jul 24 01:55:56 EDT 2025
Thu Apr 24 23:00:40 EDT 2025
Wed Aug 20 07:26:23 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 4
Keywords neutrophil extracellular traps
aging
neutrophil
periodontitis
Language English
License Attribution
http://creativecommons.org/licenses/by/3.0
2014 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c6762-18e8171764dd13a62e51f48a517f13797b12a0de8fed735a186aa5d90f51e3e93
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1111/acel.12222
PMID 24779584
PQID 1548771436
PQPubID 1036381
PageCount 9
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_4326942
proquest_miscellaneous_1549634876
proquest_journals_3227814606
proquest_journals_1548771436
gale_infotracmisc_A846991029
gale_infotracmisc_A705785025
gale_infotracacademiconefile_A846991029
gale_infotracacademiconefile_A705785025
pubmed_primary_24779584
crossref_citationtrail_10_1111_acel_12222
crossref_primary_10_1111_acel_12222
wiley_primary_10_1111_acel_12222_ACEL12222
PublicationCentury 2000
PublicationDate August 2014
PublicationDateYYYYMMDD 2014-08-01
PublicationDate_xml – month: 08
  year: 2014
  text: August 2014
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
– name: London
– name: Oxford, UK
PublicationTitle Aging cell
PublicationTitleAlternate Aging Cell
PublicationYear 2014
Publisher John Wiley & Sons, Inc
BlackWell Publishing Ltd
Publisher_xml – name: John Wiley & Sons, Inc
– name: BlackWell Publishing Ltd
References 2011; 413
2001; 70
2004; 303
1986; 70
2010; 37
2012; 188
2010; 36
2012; 167
2004; 125
2000; 67
1992; 267
2013; 63
2004; 3
2006; 8
2008; 79
2009; 113
2012; 18
2012; 16
2006; 116
2013; 8
1998; 64
2011; 18
2009; 114
2008; 140
2012; 109
1994; 65
2008; 181
2012; 91
2004; 279
2007; 176
2013; 73
2009; 184
1999; 232
2001; 33
2012; 213
2012; 7
2009; 1
2011; 29
2012; 20
2009; 15
2003; 187
2012; 119
2009; 106
e_1_2_8_28_1
Brinkmann V (e_1_2_8_5_1) 2010; 36
e_1_2_8_29_1
e_1_2_8_24_1
e_1_2_8_25_1
e_1_2_8_26_1
e_1_2_8_27_1
e_1_2_8_3_1
e_1_2_8_2_1
e_1_2_8_4_1
e_1_2_8_7_1
e_1_2_8_6_1
e_1_2_8_9_1
e_1_2_8_8_1
e_1_2_8_20_1
e_1_2_8_43_1
e_1_2_8_21_1
e_1_2_8_42_1
e_1_2_8_22_1
e_1_2_8_23_1
e_1_2_8_44_1
e_1_2_8_41_1
e_1_2_8_40_1
e_1_2_8_17_1
Dias IH (e_1_2_8_12_1) 2010; 37
e_1_2_8_18_1
e_1_2_8_39_1
e_1_2_8_19_1
e_1_2_8_13_1
e_1_2_8_36_1
e_1_2_8_14_1
e_1_2_8_35_1
e_1_2_8_15_1
e_1_2_8_38_1
e_1_2_8_16_1
e_1_2_8_37_1
e_1_2_8_32_1
e_1_2_8_10_1
e_1_2_8_31_1
e_1_2_8_11_1
e_1_2_8_34_1
e_1_2_8_33_1
e_1_2_8_30_1
References_xml – volume: 33
  start-page: 550
  year: 2001
  end-page: 555
  article-title: Fungal infections in older adults
  publication-title: Clin. Infect. Dis.
– volume: 70
  start-page: 59
  year: 1986
  end-page: 62
  article-title: Age‐related differences in granulocyte chemotaxis and degranulation
  publication-title: Clin. Sci. (Lond)
– volume: 116
  start-page: 2033
  year: 2006
  end-page: 2043
  article-title: A specific p47phox ‐serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites
  publication-title: J. Clin. Invest.
– volume: 267
  start-page: 21612
  year: 1992
  end-page: 21616
  article-title: The induction by human interleukin‐6 of apoptosis in the promonocytic cell line U937 and human neutrophils
  publication-title: J. Biol. Chem.
– volume: 167
  start-page: 261
  year: 2012
  end-page: 268
  article-title: Hypochlorous acid regulates neutrophil extracellular trap release in humans
  publication-title: Clin. Exp. Immunol.
– volume: 184
  start-page: 205
  year: 2009
  end-page: 213
  article-title: Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation
  publication-title: J. Cell Biol.
– volume: 18
  start-page: 1386
  year: 2012
  end-page: 1393
  article-title: Infection‐induced NETosis is a dynamic process involving neutrophil multitasking in vivo
  publication-title: Nat. Med.
– volume: 73
  start-page: 580
  year: 2013
  end-page: 586
  article-title: The autoantibody repertoire in periodontitis: a role in the induction of autoimmunity to citrullinated proteins in rheumatoid arthritis?
  publication-title: Ann. Rheum. Dis.
– volume: 3
  start-page: 217
  year: 2004
  end-page: 226
  article-title: Signal transduction and functional changes in neutrophils with aging
  publication-title: Aging Cell
– volume: 279
  start-page: 44123
  year: 2004
  end-page: 44132
  article-title: Induction of genes mediating interferon‐dependent extracellular trap formation during neutrophil differentiation
  publication-title: J. Biol. Chem.
– volume: 176
  start-page: 231
  year: 2007
  end-page: 241
  article-title: Novel cell death program leads to neutrophil extracellular traps
  publication-title: J. Cell Biol.
– volume: 114
  start-page: 2619
  year: 2009
  end-page: 2622
  article-title: Restoration of NET formation by gene therapy in CGD controls aspergillosis
  publication-title: Blood
– volume: 8
  start-page: 668
  year: 2006
  end-page: 676
  article-title: Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms
  publication-title: Cell. Microbiol.
– volume: 303
  start-page: 1532
  year: 2004
  end-page: 1535
  article-title: Neutrophil extracellular traps kill bacteria
  publication-title: Science
– volume: 7
  start-page: e41454
  year: 2012
  article-title: Innate immune dysfunctions in aged mice facilitate the systemic dissemination of methicillin‐resistant S. aureus
  publication-title: PLoS ONE
– volume: 181
  start-page: 5775
  year: 2008
  end-page: 5784
  article-title: Periodontitis associates with a Type 1 IFN signature in peripheral blood neutrophils
  publication-title: J. Immunol.
– volume: 29
  start-page: 1929
  year: 2011
  end-page: 1934
  article-title: Aging reduces the functionality of anti‐pneumococcal antibodies and the killing of Streptococcus pneumoniae by neutrophil phagocytosis
  publication-title: Vaccine
– volume: 67
  start-page: 40
  year: 2000
  end-page: 45
  article-title: Effect of age on human neutrophil function
  publication-title: J. Leukoc. Biol.
– volume: 106
  start-page: 6748
  year: 2009
  end-page: 6753
  article-title: Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps
  publication-title: Proc. Natl Acad. Sci. USA
– volume: 63
  start-page: 165
  year: 2013
  end-page: 197
  article-title: Neutrophil extracellular traps as a new paradigm in innate immunity: friend or foe?
  publication-title: Periodontol 2000
– volume: 36
  start-page: 1724
  year: 2010
  article-title: Neutrophil extracellular traps: how to generate and visualize them
  publication-title: J. Vis. Exp.
– volume: 70
  start-page: 881
  year: 2001
  end-page: 886
  article-title: Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans
  publication-title: J. Leukoc. Biol.
– volume: 8
  start-page: e66407
  year: 2013
  article-title: Sulforaphane restores cellular glutathione levels and reduces chronic periodontitis neutrophil hyperactivity in vitro
  publication-title: PLoS ONE
– volume: 20
  start-page: 503
  year: 2012
  end-page: 509
  article-title: Decreased phagocytic function in neutrophils and monocytes from peripheral blood in periodontal disease
  publication-title: J. Appl. Oral Sci.
– volume: 187
  start-page: 1452
  year: 2003
  end-page: 1459
  article-title: Population‐based study of the epidemiology of and the risk factors for invasive Staphylococcus aureus infections
  publication-title: J. Infect. Dis.
– volume: 1
  start-page: 225
  year: 2009
  end-page: 230
  article-title: Activation of the human contact system on neutrophil extracellular traps
  publication-title: J. Innate. Immun.
– volume: 413
  start-page: 75
  year: 2011
  end-page: 79
  article-title: Singlet oxygen is essential for neutrophil extracellular trap formation
  publication-title: Biochem. Biophys. Res. Commun.
– volume: 109
  start-page: 13076
  year: 2012
  end-page: 13081
  article-title: Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer‐associated thrombosis
  publication-title: Proc. Natl Acad. Sci. USA
– volume: 15
  start-page: 623
  year: 2009
  end-page: 625
  article-title: Netting neutrophils in autoimmune small‐vessel vasculitis
  publication-title: Nat. Med.
– volume: 91
  start-page: 369
  year: 2012
  end-page: 376
  article-title: Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide
  publication-title: J. Leukoc. Biol.
– volume: 79
  start-page: 1601
  year: 2008
  end-page: 1608
  article-title: The management of inflammation in periodontal disease
  publication-title: J. Periodontol.
– volume: 119
  start-page: 1214
  year: 2012
  end-page: 1216
  article-title: Killing by neutrophil extracellular traps: fact or folklore?
  publication-title: Blood
– volume: 140
  start-page: 255
  year: 2008
  end-page: 266
  article-title: Modern management of chronic granulomatous disease
  publication-title: Br. J. Haematol.
– volume: 37
  start-page: 1039
  year: 2010
  end-page: 1048
  article-title: Activation of the neutrophil repiratory burst by plasma from periodontitis patients is mediated by pro‐inflammatory cytokines
  publication-title: J. Clin. Periodontol.
– volume: 113
  start-page: 6419
  year: 2009
  end-page: 6427
  article-title: Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates
  publication-title: Blood
– volume: 18
  start-page: 581
  year: 2011
  end-page: 588
  article-title: Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality
  publication-title: Cell Death Differ.
– volume: 125
  start-page: 539
  year: 2004
  end-page: 546
  article-title: Role of defective ERK phosphorylation in the impaired GM‐CSF‐induced oxidative response of neutrophils in elderly humans
  publication-title: Mech. Ageing Dev.
– volume: 213
  start-page: 567
  year: 2012
  end-page: 572
  article-title: Adult Dental Health Survey 2009: common oral health conditions and their impact on the population
  publication-title: Br. Dent. J.
– volume: 65
  start-page: 260
  year: 1994
  end-page: 267
  article-title: Assessment of risk for periodontal disease. I. Risk indicators for attachment loss
  publication-title: J. Periodontol.
– volume: 232
  start-page: 3
  year: 1999
  end-page: 14
  article-title: Respiratory burst in human neutrophils
  publication-title: J. Immunol. Methods
– volume: 16
  start-page: R137
  year: 2012
  article-title: Depletion of neutrophil extracellular traps in vivo results in hypersusceptibility to polymicrobial sepsis in mice
  publication-title: Crit. Care
– volume: 64
  start-page: 537
  year: 1998
  end-page: 545
  article-title: Activation of mitogen‐activated protein kinase cascades during priming of human neutrophils by TNF‐alpha and GM‐CSF
  publication-title: J. Leukoc. Biol.
– volume: 188
  start-page: 3150
  year: 2012
  end-page: 3159
  article-title: T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses
  publication-title: J. Immunol.
– ident: e_1_2_8_33_1
  doi: 10.1016/j.vaccine.2010.12.121
– ident: e_1_2_8_19_1
  doi: 10.1038/nm.1959
– ident: e_1_2_8_22_1
  doi: 10.1042/cs0700059
– ident: e_1_2_8_14_1
  doi: 10.1083/jcb.200606027
– ident: e_1_2_8_37_1
  doi: 10.1111/j.1462-5822.2005.00659.x
– ident: e_1_2_8_11_1
  doi: 10.1073/pnas.1200419109
– volume: 36
  start-page: 1724
  year: 2010
  ident: e_1_2_8_5_1
  article-title: Neutrophil extracellular traps: how to generate and visualize them
  publication-title: J. Vis. Exp.
– ident: e_1_2_8_27_1
  doi: 10.1159/000203700
– ident: e_1_2_8_36_1
  doi: 10.1371/journal.pone.0041454
– ident: e_1_2_8_40_1
  doi: 10.1002/jlb.67.1.40
– ident: e_1_2_8_43_1
  doi: 10.1038/nm.2847
– ident: e_1_2_8_16_1
  doi: 10.1902/jop.1994.65.3.260
– ident: e_1_2_8_44_1
  doi: 10.1182/blood-2008-07-171629
– ident: e_1_2_8_42_1
  doi: 10.4049/jimmunol.181.8.5775
– ident: e_1_2_8_26_1
  doi: 10.1016/j.bbrc.2011.08.052
– volume: 37
  start-page: 1039
  year: 2010
  ident: e_1_2_8_12_1
  article-title: Activation of the neutrophil repiratory burst by plasma from periodontitis patients is mediated by pro‐inflammatory cytokines
  publication-title: J. Clin. Periodontol.
– ident: e_1_2_8_30_1
  doi: 10.1189/jlb.0711387
– ident: e_1_2_8_38_1
  doi: 10.1902/jop.2008.080173
– ident: e_1_2_8_41_1
  doi: 10.1038/sj.bdj.2012.1088
– ident: e_1_2_8_3_1
  doi: 10.1182/blood-2009-05-221606
– ident: e_1_2_8_39_1
  doi: 10.1083/jcb.200806072
– ident: e_1_2_8_17_1
  doi: 10.1073/pnas.0900226106
– ident: e_1_2_8_18_1
  doi: 10.1086/322685
– ident: e_1_2_8_8_1
  doi: 10.1111/prd.12025
– ident: e_1_2_8_35_1
  doi: 10.1016/j.mad.2004.06.001
– ident: e_1_2_8_9_1
  doi: 10.1016/S0022-1759(99)00146-5
– ident: e_1_2_8_31_1
  doi: 10.1038/cdd.2011.1
– ident: e_1_2_8_2_1
  doi: 10.1016/S0021-9258(19)36655-4
– ident: e_1_2_8_4_1
  doi: 10.1126/science.1092385
– ident: e_1_2_8_21_1
  doi: 10.1074/jbc.M405883200
– ident: e_1_2_8_15_1
  doi: 10.1111/j.1474-9728.2004.00110.x
– ident: e_1_2_8_29_1
  doi: 10.1111/j.1365-2249.2011.04518.x
– ident: e_1_2_8_6_1
  doi: 10.1189/jlb.70.6.881
– ident: e_1_2_8_25_1
  doi: 10.1186/cc11442
– ident: e_1_2_8_13_1
  doi: 10.1371/journal.pone.0066407
– ident: e_1_2_8_28_1
  doi: 10.1136/annrheumdis-2012-202701
– ident: e_1_2_8_24_1
  doi: 10.1182/blood-2011-07-364604
– ident: e_1_2_8_10_1
  doi: 10.1172/JCI27544
– ident: e_1_2_8_32_1
  doi: 10.1111/j.1365-2141.2007.06880.x
– ident: e_1_2_8_23_1
  doi: 10.1002/jlb.64.4.537
– ident: e_1_2_8_34_1
  doi: 10.4049/jimmunol.1103414
– ident: e_1_2_8_7_1
  doi: 10.1590/S1678-77572012000500002
– ident: e_1_2_8_20_1
  doi: 10.1086/374621
SSID ssj0017903
Score 2.5358407
Snippet Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune...
Neutrophil extracellular traps ( NET s) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response...
Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune response...
Summary Neutrophil extracellular traps (NETs) are a recently discovered addition to the defensive armamentarium of neutrophils, assisting in the immune...
SourceID pubmedcentral
proquest
gale
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 690
SubjectTerms Acetic acid
Adult
Age
Aged
Aging
Aging - immunology
Aging - pathology
Analysis
Bacteria
Case-Control Studies
Chronic Disease
CXCR2 protein
Defects
Disease susceptibility
Enzyme Activation - drug effects
Enzymes
Extracellular Traps - drug effects
Extracellular Traps - immunology
Female
Gum disease
Health aspects
Humans
Hypochlorous acid
Immune response
Immune system
Immunity, Innate - drug effects
Immunity, Innate - immunology
Infection
Infections
Innate immunity
Interleukin-8 - metabolism
Kinases
Leukocytes (neutrophilic)
Lipopolysaccharides
Lipopolysaccharides - pharmacology
Male
MAP kinase
Medical research
Medicine, Experimental
Microscopy
Middle Aged
neutrophil
neutrophil extracellular traps
Neutrophils
Neutrophils - drug effects
Neutrophils - immunology
Older people
Original
p38 Mitogen-Activated Protein Kinases - metabolism
Pathogens
Periodontitis
Periodontitis - immunology
Periodontitis - pathology
Proteins
Reactive oxygen species
Reactive Oxygen Species - metabolism
Receptors, Cell Surface - metabolism
Risk factors
TLR4 protein
Toll-like receptors
Tumor necrosis factor
Tumor Necrosis Factor-alpha - pharmacology
Tumor necrosis factor-TNF
SummonAdditionalLinks – databaseName: ProQuest Central
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV3da9UwFA-6IfgifnvdHBEFUahrmjRp9zKu444pOkQc7K2kTcoKpa33Y-B_v3PS3Ho7LvPpFnJuaE9Ofvmd9nwQ8h6cqlzJggWFKsFB4SIMdCjTIJelBb7OhXTt236cy7ML8e0yvvQv3BY-rHKNiQ6oTVvgO_JDR62xWbc87v4E2DUKv676Fhr3yS5AcALO1-6X2fnPX8N3BJW63shMKBGkAMO-QCnG8ujC1p8ZHI_R6Ei6DcwbJ9PtqMlNNuuOo9PH5JHnkXTaL_wTcs82T8mDvrPk32ek-wrbHNDM0MaulvO2u6pqCjg8x_upMfSUwnVHh9zFI6pp017bmhqLER60aihwQ_hpgI3SCtNILO3rPtO2pABDhlZDNtfiObk4nf0-OQt8c4WgkACAAUtswsCXk8IYxrWMbMxKkeiYwaJxlaqcRTo0NimtUTzWLJFaxyYNy5hZblP-guw0bWNfEao0OG0SmF9kjBA5TxITM6xyk1ihAYkn5ONav1nhK49jA4w6W3sg-OyZW4sJeTfIdn29ja1SH3CZMtyEqDntcwngfrCcVTZVIRbxAT73X0ngX0CRwyidkP2RJGyzYjTRtuHNf68tJvMosMj-2ezWYY5pyKCfEIbfDsM4MQa-NbZduSkAImEakHnZ29-gl0golQKBnBA1ssxBAEuHj0ea6sqVEBccM5hBj5-cDd-h6mx6Mvvurl7f_Yh75CGQSdEHR-6TneV8Zd8AYVvmB35X3gBKYD02
  priority: 102
  providerName: ProQuest
– databaseName: Wiley Online Library - Core collection (SURFmarket)
  dbid: DR2
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3di9QwEA_HgeCLnt_rnRJREIUuTZMmrfiyHHecoj6IB_ciJW1SrljSZT8O7v76m0k_3C6Lok9byDRsZie__GaZ-YWQN5BU5UoWLChUCQkKF2GgQ5kGuSwt8HUupL--7es3eXYuPl_EF3vkY98L0-pDDH-44c7weI0bXOfLjU2uC1tPGRxvCMBYrIWM6PugHYXKU766XigRpIDAnTYplvH8fnV0Gm1j8sahtF0wuUlk_Ul0ep_87NfQFqD8mq5X-bS42ZJ3_N9FHpB7HUWlszamHpA96x6SO-2lldePyPwTIAgApaHOrleLZn5Z1RQgfoGz1FjVSuF5Toe2yA9UU9dc2Zoai8UjtHIUaCd8OCC6tMIOFUtbSWnalBQQztBqaBRbPibnpyc_js-C7t6GoJCArQFLbMIgTZTCGMa1jGzMSpHomEE8cJWqnEU6NDYprVE81iyRWscmDcuYWW5T_oTsu8bZZ4QqDfmgBFIZGSNEzpPExAwFdBIrNID8hLzrf7-s6ETN8W6NOuuTG1x75j04Ia8H23kr5bHT6i2GQYb7Gz2nuzYF-D6olJXNVIj6QEAV_2oJ1A7YdxilE3I0soQdXIwm2jW8-XYfkVkHMMvMZ5p4d73cOcyxwxn8E8Lwq2EYJ8aaOmebtZ8C0BemAZunbXwPfomEUilw0wlRo8gfDFCVfDziqkuvTi44NkeDH9_7wP6Dq7PZ8ckX__T8X4wPyV1graKtwjwi-6vF2r4AZrjKX3oEuAVJQVz0
  priority: 102
  providerName: Wiley-Blackwell
Title Impaired neutrophil extracellular trap formation: a novel defect in the innate immune system of aged individuals
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Facel.12222
https://www.ncbi.nlm.nih.gov/pubmed/24779584
https://www.proquest.com/docview/1548771436
https://www.proquest.com/docview/3227814606
https://www.proquest.com/docview/1549634876
https://pubmed.ncbi.nlm.nih.gov/PMC4326942
Volume 13
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV3ra9swEBddy2Bfxt7N1gWNDcYGLpYlS_ZglLSkdGMtpSzQb0a2ZGowdpYmY_3vdyc_Gpd0-5IY7iKU093pd8k9CPkAQVWqZMa8TOUQoHDhe9qXsZfK3AJe50K68W2nZ_JkJr5fhpdbpJvf2QrwemNoh_OkZoty_8-vmwMw-K9dVo7ObLnP4KIDV7wDN5JCAz0Vt_8mqNjnbWvSIT-2AhZKxWEkBvfSXe-8dj3dTZ1ch7TuTjp-Qh63YJJOmtN_SrZs9Yw8bMZL3jwn829g6-DSDK3sarmo51dFScEZL3BrJeafUnie076A8QvVtKp_25Iai2ketKgoAER4qwCS0gJrSSxtmj_TOqfgiwwt-pKu6xdkdjz9eXTitRMWvEyCF_RYZCMQl5LCGMa1DGzIchHpkMHJcRWrlAXaNzbKrVE81CySWocm9vOQWW5j_pJsV3VldwlVGiI3CfAvMEaIlEeRCRm2uoms0OCOR-RTJ98ka9uP4xSMMunCEPzuiTuWEXnf886bphsbuT7iMSWoGyg53RYUwH6wp1UyUT528gFQ919OAGGAk_0gHpG9ASfYWjZYaBN5_dOdxiSdJicuJsQp83IjmWMtMsjHB_K7nowLY_ZbZeuVWwL8JCwDPK8a_evl0unviKiBZvYM2D98SKmKK9dHXHAsYwY5fnY6_A9RJ5Oj6Q_39PreDbwhjwBMiiY5co9sLxcr-xYA2zIdkweBOB-TncPp2fnF2P3sga8XwdjZ6V8430At
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1ba9RAFB5Ki-hL8e7WqiMqohDNJJOZRBBZ65Zdu11EWuhbnGQmNBCSuBelf8rf6Dm5uSlLferTBubsMDk58813knMh5CU4VZEUMbNimYCD4nLbUrYIrEgkBvi6y0XVvu14Jsan_OuZd7ZF_rS5MBhW2WJiBdS6iPEd-fuKWmOzbvGp_Glh1yj8utq20KjN4shc_AaXbfFx8gWe7yvHORydHIytpquAFQvY-Rbzjc_AiRFca-Yq4RiPJdxXHoPVujKQEXOUrY2fGC1dTzFfKOXpwE48ZlyDxZcA8ndgITYAwc7n0ezb9-67hQyqXsyMS24FAPtNQVSMHVKxyd4xOI6d3hF4-SBYOwkvR2mus-fq-Du8TXYb3kqHtaHdIVsmv0tu1J0sL-6RcgKwAuipaW5Wy3lRnqcZBdyf43oyDHWlcF3SLlfyA1U0L36ZjGqDESU0zSlwUfjJgf3SFNNWDK3rTNMioQB7mqZd9tjiPjm9FrU_INt5kZtHhEoFTqIApulozXnk-r72GFbV8Q1XgPwD8qbVbxg3lc6x4UYWth4P3ntYPYsBedHJlnV9j41Sr_ExhbjpUXOqyV2A9WD5rHAobSwaBPzxv5LA94CS204wIPs9SdjWcW-iTcPr_24tJmxQZxH-2yMbh11Mewb92DD8vBvGiTHQLjfFqpoCIBmmAZmHtf11enG4lAEQ1gGRPcvsBLBUeX8kT8-rkuXcxYxp0OPbyoavUHU4PBhNq6u9q2_xGbk5PjmehtPJ7OgxuQVElteBmftkezlfmSdAFpfR02aHUvLjukHhLzbWeLE
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3fi9QwEA7HHYovcv5ePTWiIAo9miZNWvFlOW-50_PwwZXDl5I2KVcoadnbPfC_dybt1u2xKD61kGnoTjKTb7Yz3xDyBoKqXMmCBYUqIUDhIgx0KNMgl6UFvM6F9O3bvp7Lk7n4fBFf7JCP61qYjh9i-MMNLcP7azTw1pQbRq4LWx8yON7AAe8hTR7s6b3pj_nP-fAVQaW-MzITSgQpOOGenhQzef48PTqQbrrljXPpZs7kJpb1h9Fsn9ztUSSddst-j-xYd5_c6vpK_npA2lMwcvBlhjq7Wi6a9rKqKXjhBb5PjYmnFO5bOlQufqCauuba1tRYzO-glaOADOHiAIvSCotILO1Yn2lTUnBChlZDLdfVQzKfHX8_Ogn61gpBIcH9BSyxCYNITgpjGNcysjErRaJjBkvGVapyFunQ2KS0RvFYs0RqHZs0LGNmuU35I7LrGmefEKo0hGwScF9kjBA5TxITM-S4SazQ4Icn5N1av1nR845j-4s6W8cf-NszvxYT8nqQbTu2ja1Sb3GZMjRB1JzuKwngfZDMKpuqECl8AM39UxLQFwDkMEon5GAkCUZWjCbaNrz59HrHZL0PuMp8MIjt5eXWYY5FyKCfEIZfDcM4Maa9Odus_BTgIGEakHnc7b9BL5FQKgX4OCFqtDMHASQOH4-46tITiAuO9cugx_d-D_9F1dn06PjM3z39H-GX5Pa3T7Ps7PT8yzNyBzCm6HImD8jucrGyzwHHLfMXvbn-BogTQQM
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Impaired+neutrophil+extracellular+trap+formation%3A+a+novel+defect+in+the+innate+immune+system+of+aged+individuals&rft.jtitle=Aging+cell&rft.au=Hazeldine%2C+Jon&rft.au=Harris%2C+Phillipa&rft.au=Chapple%2C+Iain+L&rft.au=Grant%2C+Melissa&rft.date=2014-08-01&rft.eissn=1474-9726&rft.volume=13&rft.issue=4&rft.spage=690&rft_id=info:doi/10.1111%2Facel.12222&rft_id=info%3Apmid%2F24779584&rft.externalDocID=24779584
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1474-9718&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1474-9718&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1474-9718&client=summon